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Front Matter Template Copyright by Rong Ma 2017 The Dissertation Committee for Rong Ma Certifies that this is the approved version of the following dissertation: Behavioral and Molecular Mechanisms of Pheromone Transmission in the Honey Bee (Apis mellifera) Committee: Ulrich Mueller, Supervisor Johann Hofmann Lawrence Gilbert Shalene Jha Christina Grozinger Behavioral and Molecular Mechanisms of Pheromone Transmission in the Honey Bee (Apis mellifera) by Rong Ma Dissertation Presented to the Faculty of the Graduate School of The University of Texas at Austin in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy The University of Texas at Austin August 2017 Acknowledgements At the threshold between graduate training and a professional career, I find myself reflecting on the importance of intentions. I began my PhD without a clear idea about how to join my interest in bees and chemical ecology together. It is a testament to the patience, encouragement, and guidance of my many mentors, colleagues, friends, and family that I managed any measure of success or to even complete it at all. I am deeply grateful to my advisor, Dr. Ulrich Mueller, for training me to be a careful scientist and helping me through several crises, both personal and professional, along the way. Early on, he encouraged me to spend time watching the bees, allowing my fascination with them to sustain and guide my work, which is a lesson I will not soon forget. Ulrich always had kind words of encouragement in moments of self-doubt, and I learned to trust his optimistic, yet brutally honest advice. He pushed me towards ever- greater degrees of research independence, encouraging me to find and collaborate with experts in the field. It was with his blessing that I spent much of my graduate student career in other labs, and I benefitted immeasurably from such experiences. Many thanks to my mentors, foremost among whom are the members of my dissertation committee—Drs. Larry Gilbert, Christina Grozinger, Hans Hofmann, Shalene Jha, and Ulrich Mueller—who pushed me to develop my ideas and grow as a scientist. Their comments, suggestions, and revisions greatly improved the quality of this dissertation, and I leaned on each of them through the course of my studies. I owe special thanks to Christina, who hosted me in her lab for a semester so that I could perform EAG iv experiments and learn bioinformatics methods. I am grateful to Dr. Juliana Rangel, who welcomed me into her lab for several field seasons and provided me with much guidance, support, and, importantly, all the honey bee colonies used in my experiments. Summers at the TAMU Riverside Campus, where I had all the time and space I could want to watch the bees, always held a unique calmness for me, even in the midst of hectic field seasons. I would also like the thank Dr. Bill Wcislo for giving me the opportunity to work in his lab in Panama, for making time for meandering discussions about pheromone evolution, and for introducing me to the beautiful rainforests on BCI. Big hugs all around to current and former members of the Mueller lab—Dr. Sabrina Amador-Vargas, Emma Dietrich, Chi-Chun Fang, Jake Herman, Hannah Marti, Dr. Quinn McFrederick, Zach Philips, and Dr. Chad Smith—who, in many ways, had a profound influence on my development as a scientist and as a person. While the Mueller lab was undoubtedly my academic home, I am grateful to members of the Rangel and Grozinger Labs for welcoming me into their ranks during field seasons. My heartfelt thanks to members of the Rangel lab, Dr. Adrian Fisher, Pierre Lau, Alex Payne, and Liz Walsh, for their friendship and for helping with my projects in myriad ways. Gene Ash taught me everything I know about beekeeping, which, as he might attest, may not be that much; nevertheless, my field seasons would have been complete failures without his help. I am especially indebted to Dr. Alejandra Gonzalez for holding my hand through RNA extractions, to Dr. Gabriel Villar for performing EAG experiments, and to Dr. Dave Galbraith for guiding me through transcriptome analyses. v My friends and fellow graduate students—who listened to my complaints, answered questions too embarrassingly basic for other ears, and shared in trials and tribulations—were a constant source of support, motivation, and inspiration. There are many who deserve my thanks and recognition, and I regret that I cannot list them all here. Among those I relied on most were Taylor Gullett, Luke Reding, and Chris Torres; without them, graduate school would have been a much duller experience. In the last couple years, I turned to rock climbing to maintain my sanity. Ron Safarik showed me the ropes, both literally and figuratively, and David Gawalt kept me alive despite many, many falls. By objective and conservative standards, it is safe to say that I owe them both my life. The diaspora of close friends and colleagues is a tragic and unfortunate reality of academia, but I hope that fate will bring us together again sooner than later. My parents emphasized diligence over achievement, impressing upon me from an early age that, win or lose, the trying mattered most. I am grateful to them both for this and countless other lessons, and it has been a comfort to me throughout my work and travels to have their boundless love and support, wherever I happened to be. I thank them for raising me from an early age to love books and the stories contained within them. Thanks also to Aisha for keeping me sane and grounded through dissertation writing. Her unwavering faith in me kept me going through those long months. vi Behavioral and Molecular Mechanisms of Pheromone Transmission in the Honey Bee (Apis mellifera) Rong Ma, PhD The University of Texas at Austin, 2017 Supervisor: Ulrich G. Mueller The European honey bee (Apis mellifera) has a sophisticated system of pheromonal signals that mediates a wide range of behaviors important for their fitness, including reproductive dominance, nest defense, and cooperative brood care. In honey bees, there are two distinct pheromones emitted by larvae, brood pheromone and (E)-beta-ocimene. By integrating behavior, chemical ecology, and transcriptomics, this dissertation analyzes several key stages in signal transmission in a systematic effort to understand how these two pheromones affect behavior, and in the process, generates a synthetic understanding of a highly complex system of communication. Previous studies have explored behavioral and gene expression patterns related to honey bee pheromones; however, none have compared the roles that two divergent pheromones from a common source play in rapid regulation of foraging behavior. Furthermore, while previous studies have investigated the mechanisms of pheromone detection and the factors involved in regulation of foraging behavior, it remains unclear how individual responses to pheromone exposure scales to colony-level changes in behavior. By investigating the behavioral, physiological, and genomic influences of honey bee chemical communication, this dissertation links phenotypic plasticity in behavior to gene expression profiles in the brain and provides insights into the evolution of a sophisticated chemical language. vii Table of Contents Acknowledgements ................................................................................................ iv List of Tables ......................................................................................................... xi List of Figures ....................................................................................................... xii Introduction ..............................................................................................................1 References .......................................................................................................6 Chapter 1: Assessing the Role of β-ocimene in Regulating Foraging Behavior of the Honey Bee, Apis mellifera ............................................................................10 Introduction ...................................................................................................10 Methods.........................................................................................................13 Honey bee colonies ..............................................................................13 Experimental design.............................................................................14 Synthetic pheromone and chemical analysis .......................................15 Statistical analysis ................................................................................17 RESULTS .....................................................................................................18 DISCUSSION ...............................................................................................20 Acknowledgement ........................................................................................28 References .....................................................................................................29 Chapter 2: Behavioral and Neurophysiological Mechanisms of Social Pheromone Transmission .................................................................................................32 Introduction ...................................................................................................32 METHODS: ..................................................................................................36 Experiment 1: Neurophysiological response to pheromone exposure
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